Target selection for saccadic eye movements: Direction-selective visual responses in the superior colliculus

We investigated the role of the superior colliculus (SC) in saccade target selection in rhesus monkeys who were trained to perform a direction-discrim ination task. In this task, the monkey discriminated between opposed direct ions of visual motion and indicated its judgment by making a saccadic eye m ovement to one of two visual targets that were spatially aligned with the t wo possible directions of motion in the display. Thus the neural circuits t hat implement target selection in this task are likely to receive direction ally selective visual inputs and be closely linked to the saccadic system. We therefore studied prelude neurons in the intermediate and deep layers of the SC that can discharge up to several seconds before an impending saccad e, indicating a relatively high-level role in saccade planning. We used the direction-discrimination task to identify neurons whose prelude activity " predicted" the impending perceptual report several seconds before the anima l actually executed the operant eye movement; these "choice predicting" cel ls comprised similar to 30% of the neurons we encountered in the intermedia te and deep layers of the SC. Surprisingly, about half of these prelude cel ls yielded direction-selective responses to our motion stimulus during a pa ssive fixation task. In general, these neurons responded to motion stimuli in many locations around the visual field including the center of gaze wher e the visual discriminanda were positioned during the direction-discriminat ion task. Preferred directions generally pointed toward the location of the movement field of the SC neuron in accordance with the sensorimotor demand s of the discrimination task. Control experiments indicate that the directi onal responses do not simply reflect covertly planned saccades. Our results indicate that a small population of SC prelude neurons exhibits properties appropriate for linking stimulus cues to saccade target selection in the c ontext of a visual discrimination task.